Coordinated beating of algal flagella is mediated by basal coupling

Significance In areas as diverse as developmental biology, physiology, and biomimetics, there is great interest in understanding the mechanisms by which active hair-like cellular appendages known as flagella or cilia are brought into coordinated motion. The prevailing theoretical hypothesis over many years is that fluid flows driven by beating flagella provide the coupling that leads to synchronization, but this is surprisingly inconsistent with certain experimentally observed phenomena. Here we demonstrate the insufficiency of hydrodynamic coupling in an evolutionarily significant range of unicellular algal species bearing multiple flagella, and suggest that the key additional ingredient for precise coordination of flagellar beating is provided by contractile fibers of the basal apparatus. Cilia and flagella often exhibit synchronized behavior; this includes phase locking, as seen in Chlamydomonas, and metachronal wave formation in the respiratory cilia of higher organisms. Since the observations by Gray and Rothschild of phase synchrony of nearby swimming spermatozoa, it has been a working hypothesis that synchrony arises from hydrodynamic interactions between beating filaments. Recent work on the dynamics of physically separated pairs of flagella isolated from the multicellular alga Volvox has shown that hydrodynamic coupling alone is sufficient to produce synchrony. However, the situation is more complex in unicellular organisms bearing few flagella. We show that flagella of Chlamydomonas mutants deficient in filamentary connections between basal bodies display markedly different synchronization from the wild type. We perform micromanipulation on configurations of flagella and conclude that a mechanism, internal to the cell, must provide an additional flagellar coupling. In naturally occurring species with 4, 8, or even 16 flagella, we find diverse symmetries of basal body positioning and of the flagellar apparatus that are coincident with specific gaits of flagellar actuation, suggesting that it is a competition between intracellular coupling and hydrodynamic interactions that ultimately determines the precise form of flagellar coordination in unicellular algae.